Abstract
Mosquitoes stand as a growing menace to millions of people globally as they are effectual vectors of sundry pathogens. The resurgence of mosquito-borne diseases across the world shows that the prevailing mosquito control measures are inadequate to limit the risk of those diseases properly. Aedes species, particularly Aedes aegypti and Aedes albopictus, are the vectors of arboviruses such as Dengue, Chikungunya, and Zika. Apart from being the vectors of viruses, mosquitoes host various bacterial species and indulge in symbiotic interactions with them. Several studies have revealed the significant potentialities of gut bacteria in controlling mosquitoes. A remarkably new initiative called the paratransgenesis approach plays a vital role in this area of academics. In this study, infectious arboviruses and bacterial endosymbionts of Ae. aegypti and Ae. albopictus that can endure vertical transmission have been reviewed for comprehending the role in mosquito control. This review can unravel the major vertically transmitted arboviruses and bacterial species in Aedes mosquitoes, by divulging new strategies for mosquito control.
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References
Adams B, Boots M (2010) How important is vertical transmission in mosquitoes for the persistence of dengue? Insights from a mathematical model. Epidemics 2:1–10. https://doi.org/10.1016/j.epidem.2010.01.001
Agarwal A, Dash PK, Singh AK, Sharma S, Gopalan N, Rao PV, Parida MM, Reiter P (2014) Evidence of experimental vertical transmission of emerging novel ECSA genotype of chikungunya virus in Aedes aegypti. PLoS Negl Trop Dis 8:e2990. https://doi.org/10.1371/journal.pntd.0002990
Aitken TH, Tesh RB, Beaty BJ, Rosen L (1979) Transovarial transmission of yellow fever virus by mosquitoes (Aedes aegypti). Am J Trop Med Hygiene 28:119–121. https://doi.org/10.4269/ajtmh.1979.28.119
Akhouayri IG, Habtewold T, Christophides GK (2013) Melanotic pathology and vertical transmission of the gut commensal Elizabethkingia meningoseptica in the major malaria vector Anopheles gambiae. PLoS One 8:e77619. https://doi.org/10.1371/journal.pone.0077619
Aliota MT, Peinado SA, Velez ID, Osorio JE (2016a) The wMel strain of Wolbachia reduces transmission of Zika virus by Aedes aegypti. Sci Rep 6:28792. https://doi.org/10.1038/srep28792
Aliota MT, Walker EC, Uribe Yepes A, Dario Velez I, Christensen BM, Osorio JE (2016b) The w Mel strain of Wolbachia reduces transmission of chikungunya virus in Aedes aegypti. PLoS Negl Trop Dis 10:e0004677. https://doi.org/10.1371/journal.pntd.0004677
Anderson JF, Main AJ (2006) Importance of vertical and horizontal transmission of West Nile virus by Culex pipiens in the northeastern United States. J Infect Dis 194:1577–1579. https://doi.org/10.1086/508754
Anderson JF, Main AJ, Delroux K, Fikrig E (2014) Extrinsic incubation periods for horizontal and vertical transmission of West Nile virus by Culex pipiens pipiens (Diptera: Culicidae). J Med Entomol 45:445–451. https://doi.org/10.1093/jmedent/45.3.445
Angel B, Joshi V (2009) Distribution of dengue virus types in Aedes aegypti in dengue endemic districts of Rajasthan, India. Indian J Med Res 129:665
Apte-Deshpande A, Paingankar M, Gokhale MD, Deobagkar DN (2012) Serratia odorifera a midgut inhabitant of Aedes aegypti mosquito enhances its susceptibility to dengue-2 virus. PLoS One 7:e40401. https://doi.org/10.1371/journal.pone.0040401
Apte-Deshpande AD, Paingankar MS, Gokhale MD, Deobagkar DN (2014) Serratia odorifera mediated enhancement in susceptibility of Aedes aegypti for chikungunya virus. Indian J Med Res 139:762
Arunachalam N, Tewari SC, Thenmozhi V, Rajendran R, Paramasivan R, Manavalan R, Tyagi BK (2008) Natural vertical transmission of dengue viruses by Aedes aegypti in Chennai, Tamil Nadu, India. Indian J Med Res 127:395
Bahia AC, Dong Y, Blumberg BJ, Mlambo G, Tripathi A, BenMarzouk-Hidalgo OJ, Chandra R, Dimopoulos G (2014) Exploring Anopheles gut bacteria for plasmodium blocking activity. Environ Microbiol 16:2980–2994. https://doi.org/10.1111/1462-2920.12381
Bandyopadhyay S, Lum LC, Kroeger A (2006) Classifying dengue: a review of the difficulties in using the WHO case classification for dengue haemorrhagic fever. Tropical Med Int Health 11:1238–1255. https://doi.org/10.1111/j.1365-3156.2006.01678.x
Baqar S, Hayes CG, Murphy JR, Watts DM (1993) Vertical transmission of West Nile virus by Culex and Aedes species mosquitoes. Am J Trop Med Hygiene 48:757–762
Beard C, O'Neill SL, Tesh R, Richards F, Aksoy S (1993) Modification of arthropod vector competence via symbiotic bacteria. Parasitol Today 9:179–183. https://doi.org/10.1016/0169-4758(93)90142-3
Beard CB, Cordon-Rosales C, Durvasula RV (2002) Bacterial symbionts of the triatominae and their potential use in control of Chagas disease transmission. Annu Rev Entomol 47:123–141
Beaty BJ, Tesh RB, Aitken TH (1980) Transovarial transmission of yellow fever virus in Stegomyia mosquitoes. Am J Trop Med Hygiene 29:125–132
Bennett KL, Gómez-Martínez C, Chin Y, Saltonstall K, McMillan WO, Rovira JR, Loaiza JR (2019) Dynamics and diversity of bacteria associated with the disease vectors Aedes aegypti and Aedes albopictus. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-48414-8
Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, Battle KE, Moyes CL, Henry A, Eckhoff PA, Wenger EA (2015) The effect of malaria control on plasmodium falciparum in Africa between 2000 and 2015. Nature 526:207–211. https://doi.org/10.1038/nature15535
Bian G, Xu Y, Lu P, Xie Y, Xi Z (2010) The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog 6:e1000833. https://doi.org/10.1371/journal.ppat.1000833
Bian G, Joshi D, Dong Y, Lu P, Zhou G, Pan X, Xu Y, Dimopoulos G, Xi Z (2013) Wolbachia invades Anopheles stephensi populations and induces refractoriness to plasmodium infection. Science 340:748–751. https://doi.org/10.1126/science.1236192
Billingsley P (1990) The midgut ultrastructure of hematophagous insects. Annu Rev Entomol 35:219–248. https://doi.org/10.1146/annurev.en.35.010190.001251
Binnington K, Hoffmann A (1989) Wolbachia-like organisms and cytoplasmic incompatibility in Drosophila simulans. J Invertebr Pathol 54:344–352. https://doi.org/10.1016/0022-2011(89)90118-3
Bisi DC, Lampe DJ (2011) Secretion of anti-plasmodium effector proteins from a natural Pantoea agglomerans isolate by using PelB and HlyA secretion signals. Appl Environ Microbiol 77:4669–4675. https://doi.org/10.1128/AEM.00514-11
Blagrove MS, Arias-Goeta C, Di Genua C, Failloux A-B, Sinkins SP (2013) A Wolbachia w Mel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits chikungunya virus. PLoS Negl Trop Dis 7:e2152. https://doi.org/10.1371/journal.pntd.0002152
Blitvich BJ, Firth AE (2015) Insect-specific flaviviruses: a systematic review of their discovery, host range, mode of transmission, superinfection exclusion potential and genomic organization. Viruses 7:1927–1959. https://doi.org/10.3390/v7041927
Boissière A, Tchioffo MT, Bachar D, Abate L, Marie A, Nsango SE, Shahbazkia HR, Awono-Ambene PH, Levashina EA, Christen R, Morlais I (2012) Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with plasmodium falciparum infection. PLoS Pathog 8:e1002742. https://doi.org/10.1371/journal.ppat.1002742
Bolling BG, Weaver SC, Tesh RB, Vasilakis N (2015) Insect-specific virus discovery: significance for the arbovirus community. Viruses 7:4911–4928. https://doi.org/10.3390/v7092851
Bordenstein SR, Theis KR (2015) Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13:e1002226. https://doi.org/10.1371/journal.pbio.1002226
Bosio CF, Thomas RE, Grimstad PR, Rai KS (1992) Variation in the efficiency of vertical transmission of dengue-1 virus by strains of Aedes albopictus (Diptera: Culicidae). J Med Entomol 29:985–989. https://doi.org/10.1093/jmedent/29.6.985
Bourtzis K, Dobson SL, Xi Z, Rasgon JL, Calvitti M, Moreira LA, Bossin HC, Moretti R, Baton LA, Hughes GL, Mavingui P (2014) Harnessing mosquito–Wolbachia symbiosis for vector and disease control. Acta Trop 132:S150–S163. https://doi.org/10.1016/j.actatropica.2013.11.004
Bressac C, Rousset F (1993) The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J Invertebr Pathol 61:226–230. https://doi.org/10.1006/jipa.1993.1044
Brumin M, Levy M, Ghanim M (2012) Transovarial transmission of Rickettsia spp. and organ-specific infection of the whitefly Bemisia tabaci. Appl Environ Microbiol 78:5565–5574. https://doi.org/10.1128/AEM.01184-12
Capone A, Ricci I, Damiani C, Mosca M, Rossi P, Scuppa P, Crotti E, Epis S, Angeletti M, Valzano M, Sacchi L (2013) Interactions between Asaia, plasmodium and Anopheles: new insights into mosquito symbiosis and implications in malaria symbiotic control. Parasit Vectors 6:1–13. https://doi.org/10.1186/1756-3305-6-182
Castro MGD, Nogueira RMR, Schatzmayr HG, Miagostovich MP, Lourenço-de-Oliveira R (2004) Dengue virus detection by using reverse transcription-polymerase chain reaction in saliva and progeny of experimentally infected Aedes albopictus from Brazil. Mem Inst Oswaldo Cruz 99(8):809–814. https://doi.org/10.1590/S0074-02762004000800005
Chandler LJ, Beaty BJ, Baldridge GD, Bishop DH, Hewlett MJ (1990) Heterologous reassortment of bunyaviruses in Aedes triseriatus mosquitoes and transovarial and oral transmission of newly evolved genotypes. J Gen Virol 71:1045–1050. https://doi.org/10.1099/0022-1317-71-5-1045
Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Enayati AA, Mardani N, Ghoorchian S (2012) Identification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi: a step toward finding suitable paratransgenesis candidates. Acta Trop 121:129–134. https://doi.org/10.1016/j.actatropica.2011.10.015
Chavshin AR, Oshaghi MA, Vatandoost H, Yakhchali B, Zarenejad F, Terenius O (2015) Malpighian tubules are important determinants of Pseudomonas transstadial transmission and longtime persistence in Anopheles stephensi. Parasit Vectors 8:1–7. https://doi.org/10.1186/s13071-015-0635-6
Chen W, Tsai S, Chen S, Ko Y, Fang A (1990) A study on transovarial transmission of dengue type 1 virus in Aedes aegypti. Zhonghua Minguo wei sheng wu ji mian yi xue za zhi=Chin J Microbiol Immunol 23:259–270
Chompoosri J, Thavara U, Tawatsin A, Boonserm R, Phumee A, Sangkitporn S, Siriyasatien P (2016) Vertical transmission of Indian Ocean lineage of chikungunya virus in Aedes aegypti and Aedes albopictus mosquitoes. Parasit Vectors 9(1):1–13. https://doi.org/10.1186/s13071-016-1505-6
Ciota AT, Bialosuknia SM, Zink SD, Brecher M, Ehrbar DJ, Morrissette MN, Kramer LD (2017) Effects of Zika virus strain and Aedes mosquito species on vector competence. Emerg Infect Dis 23:1110. https://doi.org/10.3201/eid2307.161633
Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA, Mulenga M, Dimopoulos G (2011) Natural microbe-mediated refractoriness to plasmodium infection in Anopheles gambiae. Science 332:855–858. https://doi.org/10.1126/science.1201618
Clancy DJ, Hoffmann AA (1998) Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans. Entomol Exp Appl 86:13–24. https://doi.org/10.1046/j.1570-7458.1998.00261.x
Clark ME, Veneti Z, Bourtzis K, Karr TL (2002) The distribution and proliferation of the intracellular bacteria Wolbachia during spermatogenesis in Drosophila. Mech Dev 111:3–15. https://doi.org/10.1016/S0925-4773(01)00594-9
Clements A (2012) Arboviruses-characteristics and concepts. The biology of mosquitoes volume 3: transmission of viruses and interactions with bacteria 4:90–173. https://doi.org/10.1079/9781845932428.0090
Coon KL, Vogel KJ, Brown MR, Strand MR (2014) Mosquitoes rely on their gut microbiota for development. Mol Ecol 23:2727–2739. https://doi.org/10.1111/mec.12771
Coon KL, Brown MR, Strand MR (2016) Mosquitoes host communities of bacteria that are essential for development but vary greatly between local habitats. Mol Ecol 25:5806–5826. https://doi.org/10.1111/mec.13877
Coon KL, Valzania L, McKinney DA, Vogel KJ, Brown MR, Strand MR (2017) Bacteria-mediated hypoxia functions as a signal for mosquito development. Proc Natl Acad Sci 114:E5362–E5369
da Costa CF, Dos Passos RA, Lima JB, Roque RA, de Souza SV, Campolina TB, Secundino NF, Pimenta PF (2017) Transovarial transmission of DENV in Aedes aegypti in the Amazon basin: a local model of xenomonitoring. Parasit Vectors 10:249. https://doi.org/10.1186/s13071-017-2194-5
Crotti E, Damiani C, Pajoro M, Gonella E, Rizzi A, Ricci I, Negri I, Scuppa P, Rossi P, Ballarini P, Raddadi N (2009) Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ Microbiol 11:3252–3264. https://doi.org/10.1111/j.1462-2920.2009.02048.x
Dada N, Jumas-Bilak E, Manguin S, Seidu R, Stenström T-A, Overgaard HJ (2014) Comparative assessment of the bacterial communities associated with Aedes aegypti larvae and water from domestic water storage containers. Parasit Vectors 7:391. https://doi.org/10.1186/1756-3305-7-391
Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126:453–465. https://doi.org/10.1016/j.cell.2006.07.014
Damiani C, Ricci I, Crotti E, Rossi P, Rizzi A, Scuppa P, Esposito F, Bandi C, Daffonchio D, Favia G (2008) Paternal transmission of symbiotic bacteria in malaria vectors. Curr Biol 18:R1087–R1088. https://doi.org/10.1016/j.cub.2008.10.040
Damiani C, Ricci I, Crotti E, Rossi P, Rizzi A, Scuppa P, Capone A, Ulissi U, Epis S, Genchi M, Sagnon NF (2010) Mosquito-bacteria symbiosis: the case of Anopheles gambiae and Asaia. Microb Ecol 60:644–654. https://doi.org/10.1007/s00248-010-9704-8
De Figueiredo ML, de C Gomes A, Amarilla AA, de S Leandro A, de S Orrico A, De Araujo RF, do SM Castro J, Durigon EL, Aquino VH, Figueiredo LT (2010) Mosquitoes infected with dengue viruses in Brazil. Virol J 7:152. https://doi.org/10.1186/1743-422X-7-152
De Freece C, Damiani C, Valzano M, D'amelio S, Cappelli A, Ricci I, Favia G (2014) Detection and isolation of the α-proteobacterium Asaia in Culex mosquitoes. Med Vet Entomol 28:438–442. https://doi.org/10.1111/mve.12045
Demaio J, Pumpuni CB, Kent M, Beier JC (1996) The midgut bacterial flora of wild Aedes triseriatus, Culex pipiens, and Psorophora columbiae mosquitoes. Am J Trop Med Hygiene 54:219–223. https://doi.org/10.4269/ajtmh.1996.54.219
Dennison NJ, Jupatanakul N, Dimopoulos G (2014) The mosquito microbiota influences vector competence for human pathogens. Curr Opin Insect Sci 3:6–13. https://doi.org/10.1016/j.cois.2014.07.004
Diallo M, Thonnon J, Fontenille D (2000) Vertical transmission of the yellow fever virus by Aedes aegypti (Diptera, Culicidae): dynamics of infection in F1 adult progeny of orally infected females. Am J Trop Med Hygiene 62:151–156. https://doi.org/10.4269/ajtmh.2000.62.151
Djadid ND, Jazayeri H, Raz A, Favia G, Ricci I, Zakeri S (2011) Identification of the midgut microbiota of an. Stephensi and an. Maculipennis for their application as a paratransgenic tool against malaria. PLoS One 6:e28484. https://doi.org/10.1371/journal.pone.0028484
Dobson SL, Marsland EJ, Rattanadechakul W (2001) Wolbachia-induced cytoplasmic incompatibility in single-and superinfected Aedes albopictus (Diptera: Culicidae). J Med Entomol 38:382–387. https://doi.org/10.1603/0022-2585-38.3.382
Dobson S, Rattanadechakul W, Marsland E (2004) Fitness advantage and cytoplasmic incompatibility in Wolbachia single-and superinfected Aedes albopictus. Heredity 93:135–142. https://doi.org/10.1038/sj.hdy.6800458
Dodson BL, Hughes GL, Paul O, Matacchiero AC, Kramer LD, Rasgon JL (2014) Wolbachia enhances West Nile virus (WNV) infection in the mosquito Culex tarsalis. PLoS Negl Trop Dis 8:e2965. https://doi.org/10.1371/journal.pntd.0002965
Dong Y, Manfredini F, Dimopoulos G (2009) Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5:e1000423. https://doi.org/10.1371/journal.ppat.1000423
Dong Y, Morton JC Jr, Ramirez JL, Souza-Neto JA, Dimopoulos G (2012) The entomopathogenic fungus Beauveria bassiana activate toll and JAK-STAT pathway-controlled effector genes and anti-dengue activity in Aedes aegypti. Insect Biochem Mol Biol 42:126–132. https://doi.org/10.1016/j.ibmb.2011.11.005
Dubrulle M, Mousson L, Moutailler S, Vazeille M, Failloux A-B (2009) Chikungunya virus and Aedes mosquitoes: saliva is infectious as soon as two days after oral infection. PLoS One 4:e5895. https://doi.org/10.1371/journal.pone.0005895
Duguma D, Rugman-Jones P, Kaufman MG, Hall MW, Neufeld JD, Stouthamer R, Walton WE (2013) Bacterial communities associated with Culex mosquito larvae and two emergent aquatic plants of bioremediation importance. PLoS One 8:e72522. https://doi.org/10.1371/journal.pone.0072522
Duguma D, Hall MW, Rugman-Jones P, Stouthamer R, Terenius O, Neufeld JD, Walton WE (2015) Developmental succession of the microbiome of Culex mosquitoes. BMC Microbiol 15:140. https://doi.org/10.1186/s12866-015-0475-8
Durvasula R, Gumbs A, Panackal A, Kruglov O, Taneja J, Kang AS, Cordon-Rosales C, Richards FF, Whitham RG, Beard CB (1999) Expression of a functional antibody fragment in the gut of Rhodnius prolixus via transgenic bacterial symbiont Rhodococcus rhodnii. Med Vet Entomol 13:115–119. https://doi.org/10.1046/j.1365-2915.1999.00175.x
Dutary BE, Leduc JW (1981) Transovarial transmission of yellow fever virus by a sylvatic vector, Haemagogus equinus. Trans R Soc Trop Med Hyg 75:128–128. https://doi.org/10.1016/0035-9203(81)90036-5
Dykstra HR, Weldon SR, Martinez AJ, White JA, Hopper KR, Heimpel GE, Asplen MK, Oliver KM (2014) Factors limiting the spread of the protective symbiont Hamiltonella defensa in Aphis craccivora aphids. Appl Environ Microbiol 80:5818–5827. https://doi.org/10.1128/AEM.01775-14
Eappen AG, Smith RC, Jacobs-Lorena M (2013) Enterobacter-activated mosquito immune responses to plasmodium involve activation of SRPN6 in Anopheles stephensi. PLoS One 8:e62937. https://doi.org/10.1371/journal.pone.0062937
Ebert D (2013) The epidemiology and evolution of symbionts with mixed-mode transmission. Annu Rev Ecol Evol Syst 44:623–643. https://doi.org/10.1146/annurev-ecolsys-032513-100555
Engel P, Moran NA (2013) The gut microbiota of insects–diversity in structure and function. FEMS Microbiol Rev 37:699–735. https://doi.org/10.1111/1574-6976.12025
Engelstädter J, Hurst GD (2009) The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40:127–149. https://doi.org/10.1146/annurev.ecolsys.110308.120206
Evans JM, Morris LS, Marchesi JR (2013) The gut microbiome: the role of a virtual organ in the endocrinology of the host. J Endocrinol 218:R37–R47. https://doi.org/10.1530/JOE-13-0131
Fang W, Vega-Rodríguez J, Ghosh AK, Jacobs-Lorena M, Kang A, Leger RJS (2011) Development of transgenic fungi that kill human malaria parasites in mosquitoes. Science 331:1074–1077. https://doi.org/10.1126/science.1199115
Fast EM, Toomey ME, Panaram K, Desjardins D, Kolaczyk ED, Frydman HM (2011) Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 334:990–992. https://doi.org/10.1126/science.1209609
Favia G, Ricci I, Damiani C, Raddadi N, Crotti E, Marzorati M, Rizzi A, Urso R, Brusetti L, Borin S, Mora D (2007) Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci 104:9047–9051. https://doi.org/10.1073/pnas.0610451104
Favia G, Ricci I, Marzorati M, Negri I, Alma A, Sacchi L, Bandi C, Daffonchio D (2008) Bacteria of the genus Asaia: a potential paratransgenic weapon against malaria. In: Aksoy S (ed) Transgenesis and the management of vector-borne disease. Advances in Experimental Medicine and Biology, vol 627. Springer, New York, pp 49–59. https://doi.org/10.1007/978-0-387-78225-6_4
Fieck A, Hurwitz I, Kang AS, Durvasula R (2010) Trypanosoma cruzi: synergistic cytotoxicity of multiple amphipathic anti-microbial peptides to T. cruzi and potential bacterial hosts. Exp Parasitol 125:342–347. https://doi.org/10.1016/j.exppara.2010.02.016
Fine PE (1975) Vectors and vertical transmission: an epidemiologic perspective. Ann N Y Acad Sci 266:173–194. https://doi.org/10.1111/j.1749-6632.1975.tb35099.x
Flores FS, Diaz LA, Batallán GP, Almirón WR, Contigiani MS (2010) Vertical transmission of St. Louis encephalitis virus in Culex quinquefasciatus (Diptera: Culicidae) in Córdoba, Argentina. Vector-Borne Zoonotic Dis 10:999–1002. https://doi.org/10.1089/vbz.2009.0136
Francy D, Rush W, Montoya M, Inglish D, Bolin R (1981) Transovarial transmission of St. Louis encephalitis virus by Culex pipiens complex mosquitoes. Am J Trop Med Hygiene 30:699–705. https://doi.org/10.1089/vbz.2009.0136
Fraser JE, De Bruyne JT, Iturbe-Ormaetxe I, Stepnell J, Burns RL, Flores HA, O’Neill SL (2017) Novel Wolbachia-transinfected Aedes aegypti mosquitoes possess diverse fitness and vector competence phenotypes. PLoS Pathog 13:e1006751. https://doi.org/10.1371/journal.ppat.1006751
Frentiu FD, Zakir T, Walker T, Popovici J, Pyke AT, van den Hurk A, McGraw EA, O'Neill SL (2014) Limited dengue virus replication in field-collected Aedes aegypti mosquitoes infected with Wolbachia. PLoS Negl Trop Dis 8:e2688. https://doi.org/10.1371/journal.pntd.0002688
Gimonneau G, Tchioffo MT, Abate L, Boissière A, Awono-Ambéné PH, Nsango SE, Christen R, Morlais I (2014) Composition of Anopheles coluzzii and Anopheles gambiae microbiota from larval to adult stages. Infect Genet Evol 28:715–724. https://doi.org/10.1016/j.meegid.2014.09.029
Gonzalez-Ceron L, Santillan F, Rodriguez MH, Mendez D, Hernandez-Avila JE (2003) Bacteria in midguts of field-collected Anopheles albimanus block plasmodium vivax sporogonic development. J Med Entomol 40:371–374. https://doi.org/10.1603/0022-2585-40.3.371
Gubler DJ, Rosen L (1976) Variation among geographic strains of Aedes albopictus in suceptibility to infection with dengue viruses. Am J Trop Med Hygiene 25:318–325. https://doi.org/10.4269/ajtmh.1976.25.318
Gubler DJ, Nalim S, Tan R, Saipan H, Saroso JS (1979) Variation in susceptibility to oral infection with dengue viruses among geographic strains of Aedes aegypti. Am J Trop Med Hygiene 28:1045–1052. https://doi.org/10.4269/ajtmh.1979.28.1045
Guégan M, Zouache K, Démichel C, Minard G, Potier P, Mavingui P, Moro CV (2018) The mosquito holobiont: fresh insight into mosquito-microbiota interactions. Microbiome 6:1–17. https://doi.org/10.1186/s40168-018-0435-2
Guo X, Li C, Deng Y, Jiang Y, Sun A, Liu Q, Zhao T (2020) Vector competence and vertical transmission of Zika virus in Aedes albopictus (Diptera: Culicidae). Vector-Borne Zoonotic Dis 20:374–379. https://doi.org/10.1089/vbz.2019.2492
Gusmão DS, Santos AV, Marini DC, Bacci M Jr, Berbert-Molina MA, Lemos FJA (2010) Culture-dependent and culture-independent characterization of microorganisms associated with Aedes aegypti (Diptera: Culicidae)(L.) and dynamics of bacterial colonization in the midgut. Acta Trop 115:275–281. https://doi.org/10.1016/j.actatropica.2010.04.011
Hadfield SJ, Axton JM (1999) Germ cells colonized by endosymbiotic bacteria. Nature 402:482–482. https://doi.org/10.1038/45002
Harbach RE, Besansky NJ (2014) Mosquitoes. Curr Biol 24:R14–R15. https://doi.org/10.1016/j.cub.2013.09.047
Hardy JL, Apperson G, Asman SM, Reeves WC (1978) Selection of a strain of Culex tarsalis highly resistant to infection following ingestion of western equine encephalomyelitis virus. Am J Trop Med Hygiene 27:313–321. https://doi.org/10.4269/ajtmh.1978.27.313
Hardy JL, Rosen L, Kramer LD, Presser SB, Shroyer DA, Turell MJ (1980) Effect of rearing temperature on transovarial transmission of St. Louis encephalitis virus in mosquitoes. Am J Trop Med Hygiene 29:963–968. https://doi.org/10.4269/ajtmh.1980.29.963
Hardy JL, Houk EJ, Kramer LD, Reeves WC (1983) Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol 28:229–262. https://doi.org/10.1146/annurev.en.28.010183.001305
Hardy JL, Rosen L, Reeves WC, Scrivani RP, Presser SB (1984) Experimental transovarial transmission of St. Louis encephalitis virus by Culex and Aedes mosquitoes. Am J Trop Med Hygiene 33:166–175. https://doi.org/10.4269/ajtmh.1984.33.166
Herren JK, Paredes JC, Schüpfer F, Lemaitre B (2013) Vertical transmission of a Drosophila endosymbiont via cooption of the yolk transport and internalization machinery. MBio 4. https://doi.org/10.1128/mBio.00532-12
Higgs S, Beaty BJ (2005) Natural cycles of vector-borne pathogens. Biol Dis Vectors:167–186
Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, Greenfield M, Durkan M, Leong YS, Dong Y, Cook H (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454–457. https://doi.org/10.1038/nature10356
Hoffmann AA, Iturbe-Ormaetxe I, Callahan AG, Phillips BL, Billington K, Axford JK, Montgomery B, Turley AP, O'Neill SL (2014) Stability of the w Mel Wolbachia infection following invasion into Aedes aegypti populations. PLoS Negl Trop Dis 8:e3115. https://doi.org/10.1371/journal.pntd.0003115
Hogenhout SA, Ammar E-D, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359. https://doi.org/10.1146/annurev.phyto.022508.092135
Hughes GL, Rasgon JL (2014) Transinfection: a method to investigate W olbachia–host interactions and control arthropod-borne disease. Insect Mol Biol 23:141–151. https://doi.org/10.1111/imb.12066
Hughes GL, Koga R, Xue P, Fukatsu T, Rasgon JL (2011) Wolbachia infections are virulent and inhibit the human malaria parasite plasmodium falciparum in Anopheles gambiae. PLoS Pathog 7:e1002043. https://doi.org/10.1371/journal.ppat.1002043
Hughes GL, Dodson BL, Johnson RM, Murdock CC, Tsujimoto H, Suzuki Y, Patt AA, Cui L, Nossa CW, Barry RM, Sakamoto JM (2014) Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes. Proc Natl Acad Sci 111:12498–12503. https://doi.org/10.1073/pnas
Hull B, Tikasingh E, de Souza M, Martinez R (1984) Natural transovarial transmission of dengue 4 virus in Aedes aegypti in Trinidad. Am J Trop Med Hygiene 33:1248–1250. https://doi.org/10.4269/ajtmh.1984.33.1248
Ijichi N, Kondo N, Matsumoto R, Shimada M, Ishikawa H, Fukatsu T (2002) Internal spatiotemporal population dynamics of infection with three Wolbachia strains in the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). Appl Environ Microbiol 68:4074–4080. https://doi.org/10.1128/AEM.68.8.4074-4080.2002
Jiggins FM (2017) The spread of Wolbachia through mosquito populations. PLoS Biol 15:e2002780. https://doi.org/10.1371/journal.pbio.2002780
Joshi V, Mourya D, Sharma R (2002) Persistence of dengue-3 virus through transovarial transmission passage in successive generations of Aedes aegypti mosquitoes. Am J Trop Med Hygiene 67:158–161. https://doi.org/10.4269/ajtmh.2002.67.158
Jousset (1981) F-X Geographic Aedes aegypti strains and dengue-2 virus: susceptibility, ability to transmit to vertebrate and transovarial transmission. In: Annales de l’Institut Pasteur/Virologie. Elsevier 132(3):357–370. https://doi.org/10.1016/S0769-2617(81)80006-8
Jupatanakul N, Sim S, Dimopoulos G (2014) The insect microbiome modulates vector competence for arboviruses. Viruses 6:4294–4313. https://doi.org/10.3390/v6114294
Kambris Z, Cook PE, Phuc HK, Sinkins SP (2009) Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326:134–136. https://doi.org/10.1126/science.1177531
Kay B, Carley J (1980) ©Transovarial transmission of murray valley encephalitis virus by Aedes aegypti (L.). Aust J Exp Biol Med Sci 58(5):429–532. https://doi.org/10.1038/icb.1980.51
Khin MM, Than KA (1983) Transovarial transmission of dengue 2 virus by Aedes aegypti in nature. Am J Trop Med Hygiene 32:590–594. https://doi.org/10.4269/ajtmh.1983.32.590
Kose H, Karr TL (1995) Organization of Wolbachia pipientis in the Drosophila fertilized egg and embryo revealed by an anti-Wolbachia monoclonal antibody. Mech Dev 51:275–288. https://doi.org/10.1016/0925-4773(95)00372-X
Larsen JR, Ashley RF (1971) Demonstration of Venezuelan equine encephalomyelitis virus in tissues of Aedes aegypti. Am J Trop Med Hygiene 20:754–760. https://doi.org/10.4269/ajtmh.1971.20.754
Leake CJ (1984) Transovarial transmission of arboviruses by mosquitoes. Vectors in virus biology, In, pp 63–91
Lee H, Rohani A (2005) Transovarial transmission of dengue virus in Aedes aegypti and Aedes albopictus in relation to dengue outbreak in an urban area in Malaysia. WHO Regional Office for South-East Asia. Dengue Bulletin 29. Available at https://apps.who.int/iris/bitstream/handle/10665/164121/dbv29p106.pdf. Accessed 02 April 2022
Lee HL, Mustafakamal I, Rohani A (1997) Does transovarial transmission of dengue virus occur in Malaysian Aedes aegypti and Aedes albopictus? Southeast Asian J Trop Med Public Health 28:230–232
Lequime S, Paul RE, Lambrechts L (2016) Determinants of arbovirus vertical transmission in mosquitoes. PLoS Pathog 12:e1005548. https://doi.org/10.1371/journal.ppat.1005548
Lipsitch M, Siller S, Nowak MA (1996) The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50:1729–1741. https://doi.org/10.1111/j.1558-5646.1996.tb03560.x
Lutomiah JJ, Mwandawiro C, Magambo J, Sang RC (2007) Infection and vertical transmission of Kamiti river virus in laboratory bred Aedes aegypti mosquitoes J Insect Sci 7. https://doi.org/10.1673/031.007.5501
Maia LMS, Bezerra MCF, Costa MCS, Souza EM, Oliveira MEB, Ribeiro ALM, Slhessarenko RD (2019) Natural vertical infection by dengue virus serotype 4, Zika virus and Mayaro virus in Aedes (Stegomyia) aegypti and Aedes (Stegomyia) albopictus. Med Vet Entomol 33:437–442. https://doi.org/10.1111/mve.12369
Mancini MV, Damiani C, Accoti A, Tallarita M, Nunzi E, Cappelli A, Bozic J, Catanzani R, Rossi P, Valzano M, Serrao A (2018) Estimating bacteria diversity in different organs of nine species of mosquito by next generation sequencing. BMC Microbiol 18:1–10. https://doi.org/10.1186/s12866-018-1266-9
Martins VEP, Alencar CH, Kamimura MT, de Carvalho Araujo FM, De Simone SG, Dutra RF, Guedes MIF (2012) Occurrence of natural vertical transmission of dengue-2 and dengue-3 viruses in Aedes aegypti and Aedes albopictus in Fortaleza, Ceará, Brazil. PLoS One 7:e41386. https://doi.org/10.1371/journal.pone.0041386
McGraw EA, O'neill SL (2013) Beyond insecticides: new thinking on an ancient problem. Nat Rev Microbiol 11:181–193. https://doi.org/10.1038/nrmicro2968
McMeniman CJ, Lane RV, Cass BN, Fong AW, Sidhu M, Wang Y-F, O'Neill SL (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323:141–144. https://doi.org/10.1126/science.1165326
Messenger SL, Molineux IJ, Bull J (1999) Virulence evolution in a virus obeys a trade off. Proc R Soc Lond Ser B Biol Sci 266:397–404. https://doi.org/10.1098/rspb.1999.0651
Miller N, Lehane M (1993) Peritrophic membranes, cell surface molecules and parasite tropisms within arthropod vectors. Parasitol Today 9:45–50. https://doi.org/10.1016/0169-4758(93)90030-J
Miller B, DeFoliart G, Yuill T (1979) Aedes triseriatus and La Crosse virus: lack of infection in eggs of the first ovarian cycle following oral infection of females. Am J Trop Med Hygiene 28:897–901. https://doi.org/10.4269/ajtmh.1979.28.897
Miller BR, Nasci RS, Godsey MS, Savage HM, Lutwama JJ, Lanciotti RS, Peters CJ (2000) First field evidence for natural vertical transmission of West Nile virus in Culex univittatus complex mosquitoes from Rift Valley province, Kenya. Am J Trop Med Hygiene 62:240–246. https://doi.org/10.4269/ajtmh.2000.62.240
Minard G, Mavingui P, Moro CV (2013) Diversity and function of bacterial microbiota in the mosquito holobiont. Parasit Vectors 6:1–12. https://doi.org/10.1186/1756-3305-6-146
Mink G (1993) Pollen and seed-transmitted viruses and viroids. Annu Rev Phytopathol 31:375–402. https://doi.org/10.1146/annurev.py.31.090193.002111
Mitchell C, Miller B (1990) Vertical transmission of dengue viruses by strains of Aedes albopictus recently introduced into. Braz J Am Mosq Control Assoc 6:251–253
Mohanty I, Rath A, Mahapatra N, Hazra RK (2016) Wolbachia: A biological control strategy against arboviral diseases. J Vector Borne Dis 53:199
Moreira LA, Ghosh AK, Abraham EG, Jacobs-Lorena M (2002) Genetic transformation of mosquitoes: a quest for malaria control. Int J Parasitol 32:1599–1605. https://doi.org/10.1016/S0020-7519(02)00188-1
Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, Rocha BC, Hall-Mendelin S, Day A, Riegler M, Hugo LE (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and plasmodium. Cell 139:1268–1278. https://doi.org/10.1016/j.cell.2009.11.042
Mourya D (1987) Absence of transovarial transmission of chikungunya virus in Aedes aegypti× ae. Albopictus mosquitoes. Indian J Med Res 85:593–595
Mourya DT, Gokhale MD, Basu A, Barde PV, Sapkal GN, Padbidri VS, Gore MM (2001) Horizontal and vertical transmission of dengue virus type 2 in highly and lowly susceptible strains of Aedes aegypti mosquitoes. Acta Virol 45:67–72
Moya A, Peretó J, Gil R, Latorre A (2008) Learning how to live together: genomic insights into prokaryote–animal symbioses. Nat Rev Genet 9:218–229. https://doi.org/10.1038/nrg2319
Muturi EJ, Lagos-Kutz D, Dunlap C, Ramirez JL, Rooney AP, Hartman GL, Fields CJ, Rendon G, Kim CH (2018) Mosquito microbiota cluster by host sampling location. Parasit Vectors 11:468. https://doi.org/10.1186/s13071-018-3036-9
Newton IL, Savytskyy O, Sheehan KB (2015) Wolbachia utilize host actin for efficient maternal transmission in Drosophila melanogaster. PLoS Pathog 11:e1004798. https://doi.org/10.1371/journal.ppat.1004798
Ngwa C, Glöckner V, Abdelmohsen UR, Scheuermayer M, Fischer R, Hentschel U, Pradel G (2013) 16S rRNA gene-based identification of Elizabethkingia meningoseptica (Flavobacteriales: Flavobacteriaceae) as a dominant midgut bacterium of the Asian malaria vector Anopheles stephensi (Dipteria: Culicidae) with antimicrobial activities. J Med Entomol 50:404–414. https://doi.org/10.1603/ME12180
Okech BA, Gouagna LC, Yan G, Githure JI, Beier JC (2007) Larval habitats of Anopheles gambiae ss (Diptera: Culicidae) influences vector competence to Plasmodium falciparum parasites. Malar J 6:1–7. https://doi.org/10.1186/1475-2875-6-50
Olson K, Myles K, Seabaugh R, Higgs S, Carlson J, Beaty B (2000) Development of a Sindbis virus expression system that efficiently expresses green fluorescent protein in midguts of Aedes aegypti following per os infection. Insect Mol Biol 9:57–65. https://doi.org/10.1046/j.1365-2583.2000.00162.x
O'Neill SL, Giordano R, Colbert A, Karr TL, Robertson HM (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci 89:2699–2702. https://doi.org/10.1073/pnas.89.7.2699
Pidiyar V, Kaznowski A, Narayan NB, Patole M, Shouche YS (2002) Aeromonas culicicola sp. nov., from the midgut of Culex quinquefasciatus. Int J Syst Evol Microbiol 52:1723–1728. https://doi.org/10.1099/00207713-52-5-1723
Pidiyar VJ, Jangid K, Patole MS, Shouche YS (2004) Studies on cultured and uncultured microbiota of wild Culex quinquefasciatus mosquito midgut based on 16S ribosomal RNA gene analysis. Am J Trop Med Hygiene 70:597–603. https://doi.org/10.4269/ajtmh.2004.70.597
Pierro D, Myles K, Foy B, Beaty B, Olson K (2003) Development of an orally infectious Sindbis virus transducing system that efficiently disseminates and expresses green fluorescent protein in Aedes aegypti. Insect Mol Biol 12:107–116. https://doi.org/10.1046/j.1365-2583.2003.00392.x
Pumpuni CB, Beier MS, Nataro JP, Guers LD, Davis J (1993) Plasmodium falciparum: inhibition of sporogonic development in Anopheles stephensi by gram-negative bacteria. Exp Parasitol 77:195–199. https://doi.org/10.1006/expr.1993.1076
Pumpuni CB, Demaio J, Kent M, Davis JR, Beier JC (1996) Bacterial population dynamics in three anopheline species: the impact on plasmodium sporogonic development. Am J Trop Med Hygiene 54:214–218. https://doi.org/10.4269/ajtmh.1996.54.214
Ramirez JL, Souza-Neto J, Cosme RT, Rovira J, Ortiz A, Pascale JM, Dimopoulos G (2012) Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLoS Negl Trop Dis 6:e1561. https://doi.org/10.1371/journal.pntd.0001561
Ramirez JL et al (2014) Chromobacterium Csp_P reduces malaria and dengue infection in vector mosquitoes and has entomopathogenic and in vitro anti-pathogen activities. PLoS Pathog 10:e1004398. https://doi.org/10.1371/journal.ppat.1004398
Rani A, Sharma A, Rajagopal R, Adak T, Bhatnagar RK (2009) Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiol 9:96. https://doi.org/10.1186/1471-2180-9-96
Ren X, Hoiczyk E, Rasgon JL (2008) Viral paratransgenesis in the malaria vector Anopheles gambiae. PLoS Pathog 4:e1000135. https://doi.org/10.1371/journal.ppat.1000135
Ricci I, Valzano M, Ulissi U, Epis S, Cappelli A, Favia G (2012) Symbiotic control of mosquito borne disease. Pathogens Glob Health 106:380–385. https://doi.org/10.1179/2047773212Y.0000000051
Riehle MA, Jacobs-Lorena M (2005) Using bacteria to express and display anti-parasite molecules in mosquitoes: current and future strategies. Insect Biochem Mol Biol 35:699–707. https://doi.org/10.1016/j.ibmb.2005.02.008
Riehle MA, Moreira CK, Lampe D, Lauzon C, Jacobs-Lorena M (2007) Using bacteria to express and display anti-plasmodium molecules in the mosquito midgut. Int J Parasitol 37:595–603. https://doi.org/10.1016/j.ijpara.2006.12.002
Romoser WS, Wasieloski LP Jr, Pushko P, Kondig JP, Lerdthusnee K, Neira M, Ludwig GV (2004) Evidence for arbovirus dissemination conduits from the mosquito (Diptera: Culicidae) midgut. J Med Entomol 41:467–475. https://doi.org/10.1603/0022-2585-41.3.467
Rosen L (1987) Mechanism of vertical transmission of the dengue virus in mosquitoes. C R Acad Sci III Sci Vie 304:347
Rosen L (1988) Further observations on the mechanism of vertical transmission of flaviviruses by Aedes mosquitoes. Am J Trop Med Hygiene 39:123–126. https://doi.org/10.4269/ajtmh.1988.39.123
Rosen L, Tesh RB, Lien JC, Cross JH (1978) Transovarial transmission of Japanese encephalitis virus by mosquitoes. Science 199:909–911. https://doi.org/10.1126/science.203035
Rosen L, Shroyer DA, Tesh RB, Freier JE, Lien JC (1983) Transovarial transmission of dengue viruses by mosquitoes: Aedes albopictus and Aedes aegypti. Am J Trop Med Hygiene 32:1108–1119. https://doi.org/10.4269/ajtmh.1983.32.1108
Rosen L, Roseboom LE, Gubler DJ, Lien JC, Chaniotis BN (1985) Comparative susceptibility of mosquito species and strains to oral and parenteral infection with dengue and Japanese encephalitis viruses. Am J Trop Med Hygiene 34:603–615. https://doi.org/10.4269/ajtmh.1985.34.603
Rosen L, Lien J-C, Shroyer DA, Baker RH, Lu L-C (1989) Experimental vertical transmission of Japanese encephalitis virus by Culex tritaeniorhynchus and other mosquitoes. Am J Trop Med Hygiene 40:548–556
Rosenberg R, Lindsey NP, Fischer M, Gregory CJ, Hinckley AF, Mead PS, Paz-Bailey G, Waterman SH, Drexler NA, Kersh GJ, Hooks H (2018) Vital signs: trends in reported vectorborne disease cases—United States and territories, 2004–2016. Morb Mortal Wkly Rep 67:496. https://doi.org/10.15585/mmwr.mm6717e1
Rossi P, Ricci I, Cappelli A, Damiani C, Ulissi U, Mancini MV, Valzano M, Capone A, Epis S, Crotti E, Chouaia B (2015) Mutual exclusion of Asaia and Wolbachia in the reproductive organs of mosquito vectors. Parasit Vectors 8:1–10. https://doi.org/10.1186/s13071-015-0888-0
Rousset F, Raymond M (1991) Cytoplasmic incompatibility in insects: why sterilize females? Trends Ecol Evol 6:54–57. https://doi.org/10.1016/0169-5347(91)90123-F
Rousset F, Bouchon D, Pintureau B, Juchault P, Solignac M (1992) Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc R Soc Lond Ser B Biol Sci 250:91–98. https://doi.org/10.1098/rspb.1992.0135
Ruang-areerate T, Kittayapong P (2006) Wolbachia transinfection in Aedes aegypti: a potential gene driver of dengue vectors. Proc Natl Acad Sci 103:12534–12539. https://doi.org/10.1073/pnas.0508879103
Saiyasombat R, Bolling BG, Brault AC, Bartholomay LC, Blitvich BJ (2011) Evidence of efficient transovarial transmission of Culex flavivirus by Culex pipiens (Diptera: Culicidae). J Med Entomol 48:1031–1038. https://doi.org/10.1603/ME11043
Saldaña MA, Hegde S, Hughes GL (2017) Microbial control of arthropod-borne disease. Mem Inst Oswaldo Cruz 112:81–93. https://doi.org/10.1590/0074-02760160373
Saridaki A, Bourtzis K (2010) Wolbachia: more than just a bug in insects genitals. Curr Opin Microbiol 13:67–72. https://doi.org/10.1016/j.mib.2009.11.005
Scott TW, Weaver SC, Mallampalli VL (1994) Evolution of mosquito-borne viruses. Evol Biol Viruses 293:324
Sharma P, Sharma S, Maurya RK, De TD, Thomas T, Lata S, Singh N, Pandey KC, Valecha N, Dixit R (2014) Salivary glands harbor more diverse microbial communities than gut in Anopheles culicifacies. Parasit Vectors 7:1–7. https://doi.org/10.1186/1756-3305-7-235
Shroyer DA (1986) Transovarial maintenance of San Angelo virus in sequential generations of Aedes albopictus. Am J Trop Med Hygiene 35:408–417. https://doi.org/10.4269/ajtmh.1986.35.408
Shroyer DA (1990) Vertical maintenance of dengue-1 virus in sequential generations of Aedes albopictus. J Am Mosq Control Assoc 6:312–314
Sinkins SP (2004) Wolbachia and cytoplasmic incompatibility in mosquitoes. Insect Biochem Mol Biol 34:723–729. https://doi.org/10.1016/j.ibmb.2004.03.025
Sinkins S, Braig H, O'Neill SL (1995) Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proc R Soc Lond Ser B Biol Sci 261:325–330. https://doi.org/10.1098/rspb.1995.0154
Smith DR, Arrigo NC, Leal G, Muehlberger LE, Weaver SC (2007) Infection and dissemination of Venezuelan equine encephalitis virus in the epidemic mosquito vector, Aedes taeniorhynchus. Am J Trop Med Hygiene 77:176–187. https://doi.org/10.4269/ajtmh.2007.77.176
Stewart AD, Logsdon JM, Kelley SE (2005) An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59:730–739. https://doi.org/10.1111/j.0014-3820.2005.tb01749.x
Stouthamer R, Breeuwer JA, Hurst GD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102. https://doi.org/10.1146/annurev.micro.53.1.71
Straif SC, Mbogo CN, Toure AM, Walker ED, Kaufman M, Toure YT, Beier JC (1998) Midgut bacteria in Anopheles gambiae and an. Funestus (Diptera: Culicidae) from Kenya and Mali. J Med Entomol 35:222–226. https://doi.org/10.1093/jmedent/35.3.222
Takken W, Smallegange RC, Vigneau AJ, Johnston V, Brown M, Mordue-Luntz AJ, Billingsley PF (2013) Larval nutrition differentially affects adult fitness and plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi. Parasit Vectors 6:1–10. https://doi.org/10.1186/1756-3305-6-345
Tesh RB (1980) Experimental studies on the transovarial transmission of Kunjin and San Angelo viruses in mosquitoes. Am J Trop Med Hygiene 29:657–666. https://doi.org/10.4269/ajtmh.1980.29.657
Tesh R (1984) Transovarial transmission of arboviruses in their invertebrate vectors. Curr Top Vector Res 2:57–76
Tesh RB, Cornet M (1981) The location of San Angelo virus in developing ovaries of transovarially infected Aedes albopictus mosquitoes as revealed by fluorescent antibody technique. Am J Trop Med Hygiene 30:212–218. https://doi.org/10.4269/ajtmh.1981.30.212
Tesh RB, Gubler DJ (1975) Laboratory studies of transovarial transmission of La Crosse and other arboviruses by Aedes albopictus and Culex fatigans. Am J Trop Med Hygiene 24:876–880. https://doi.org/10.4269/ajtmh.1975.24.876
Tesh RB, Shroyer DA (1980) The mechanism of arbovirus transovarial transmission in mosquitoes: San Angelo virus in Aedes albopictus. Am J Trop Med Hygiene 29:1394–1404. https://doi.org/10.4269/ajtmh.1980.29.1394
Tesh RB, Gubler DJ, Rosen L (1976) Variation among geographic strains of Aedes albopictus in susceptibility to infection with chikungunya virus. Am J Trop Med Hygiene 25:326–335. https://doi.org/10.4269/ajtmh.1976.25.326
Tesh R, Bolling B, Beaty B (2016) Role of vertical transmission in arbovirus maintenance and evolution. Arboviruses: Molecular Biology, Evolution and Control 13:191–218. https://doi.org/10.21775/9781910190210.13
Thangamani S, Huang J, Hart CE, Guzman H, Tesh RB (2016) Vertical transmission of Zika virus in Aedes aegypti mosquitoes. Am J Trop Med Hygiene 95:1169–1173. https://doi.org/10.4269/ajtmh.16-0448
Thenmozhi V, Hiriyan JG, Tewari SC, Samuel PP, Paramasivan R, Rajendran R, Tyagi BK (2007) Natural vertical transmission of dengue virus in Aedes albopictus (Diptera: Culicidae) in Kerala, a southern Indian state. Jpn J Infect Dis 60:245
Thongsripong P, Chandler JA, Green AB, Kittayapong P, Wilcox BA, Kapan DD, Bennett SN (2018) Mosquito vector-associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod-borne diseases. Ecol Evol 8:1352–1368. https://doi.org/10.1002/ece3.3676
Touré AM, Mackey AJ, Wang ZX, Beier JC (2000) Bactericidal effects of sugar-fed antibiotics on resident midgut bacteria of newly emerged anopheline mosquitoes (Diptera: Culicidae). J Med Entomol 37:246–249. https://doi.org/10.1093/jmedent/37.2.246
Tram U, Ferree PM, Sullivan W (2003) Identification of Wolbachia–host interacting factors through cytological analysis. Microbes Infect 5:999–1011. https://doi.org/10.1016/S1286-4579(03)00192-8
Turell MJ (1988) Horizontal and vertical transmission of viruses by insect and tick vectors. Arboviruses Epidemiol Ecol 1:127–152
Turelli M, Hoffmann AA (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140:1319–1338
Turner PE, Cooper VS, Lenski RE (1998) Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution 52:315–329. https://doi.org/10.1111/j.1558-5646.1998.tb01634.x
Van den Hurk AF et al (2012) Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. PLoS Negl Trop Dis 6:e1892. https://doi.org/10.1371/journal.pntd.0001892
Vazeille M, Mousson L, Failloux A-B (2009) Failure to demonstrate experimental vertical transmission of the epidemic strain of chikungunya virus in Aedes albopictus from La Réunion Island, Indian Ocean. Mem Inst Oswaldo Cruz 104:632–635. https://doi.org/10.1590/S0074-02762009000400017
Wang S, Jacobs-Lorena M (2013) Genetic approaches to interfere with malaria transmission by vector mosquitoes. Trends Biotechnol 31:185–193. https://doi.org/10.1016/j.tibtech.2013.01.001
Wang Y, Gilbreath TM III, Kukutla P, Yan G, Xu J (2011) Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PLoS One 6:e24767. https://doi.org/10.1371/journal.pone.0024767
Wang S, Ghosh AK, Bongio N, Stebbings KA, Lampe DJ, Jacobs-Lorena M (2012) Fighting malaria with engineered symbiotic bacteria from vector mosquitoes. Proc Natl Acad Sci 109:12734–12739. https://doi.org/10.1073/pnas.1204158109
Wang S, Dos-Santos AL, Huang W, Liu KC, Oshaghi MA, Wei G, Agre P, Jacobs-Lorena M (2017) Driving mosquito refractoriness to plasmodium falciparum with engineered symbiotic bacteria. Science 357:1399–1402. https://doi.org/10.1126/science.aan5478
Watts D, Eldridge B (1975) Transovarial transmission of arboviruses by mosquitoes: a review. Med Biol 53:271
Werren JH (1997) Biology of wolbachia. Annu Rev Entomol 42:587–609. https://doi.org/10.1146/annurev.ento.42.1.587
Werren JH, Zhang W, Guo LR (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc R Soc Lond Ser B Biol Sci 261:55–63. https://doi.org/10.1098/rspb.1995.0117
Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751. https://doi.org/10.1038/nrmicro1969
Wilkinson T, Fukatsu T, Ishikawa H (2003) Transmission of symbiotic bacteria Buchnera to parthenogenetic embryos in the aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Arthropod Struct Dev 32:241–245. https://doi.org/10.1016/S1467-8039(03)00036-7
Woodring J, Chandler LJ, Oray CT, McGaw MM, Blair CD, Beaty BJ (1998) Diapause, transovarial transmission, and filial infection rates in geographic strains of La Crosse virus-infected Aedes triseriatus. Am J Trop Med Hygiene 58:587–588. https://doi.org/10.4269/ajtmh.1998.58.587
Xi Z, Khoo CC, Dobson SL (2005) Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310:326–328. https://doi.org/10.1126/science.1117607
Xi Z, Ramirez JL, Dimopoulos G (2008) The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 4:e1000098. https://doi.org/10.1371/journal.ppat.1000098
Yoshida S, Ioka D, Matsuoka H, Endo H, Ishii A (2001) Bacteria expressing single-chain immunotoxin inhibit malaria parasite development in mosquitoes. Mol Biochem Parasitol 113:89–96. https://doi.org/10.1016/S0166-6851(00)00387-X
Zouache K, Voronin D, Tran-Van V, Mousson L, Failloux A-B, Mavingui P (2009) Persistent Wolbachia and cultivable bacteria infection in the reproductive and somatic tissues of the mosquito vector Aedes albopictus. PLoS One 4:e6388. https://doi.org/10.1371/journal.pone.0006388
Zouache K, Raharimalala FN, Raquin V, Tran-Van V, Raveloson LHR, Ravelonandro P, Mavingui P (2011) Bacterial diversity of field-caught mosquitoes, Aedes albopictus and Aedes aegypti, from different geographic regions of Madagascar. FEMS Microbiol Ecol 75:377–389. https://doi.org/10.1111/j.1574-6941.2010.01012.x
Zug R, Hammerstein P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol Rev 90:89–111. https://doi.org/10.1111/brv.12098
Acknowledgments
The authors would like to thank Department of Zoology, University of Calicut for the laboratory facilities provided. The authors offer sincere gratitude to the University Grants Commission, Government of India for financial support of the author Kaavya K. in the form of UGC Junior Research Fellowship.
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Kaavya, K., Tharakan, J., Joshi, C.O. et al. Role of vertically transmitted viral and bacterial endosymbionts of Aedes mosquitoes. Does Paratransgenesis influence vector-borne disease control?. Symbiosis 86, 139–153 (2022). https://doi.org/10.1007/s13199-022-00836-1
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DOI: https://doi.org/10.1007/s13199-022-00836-1